Reproductive Coordination in a Nonseasonally Breeding Primate Species,Macaca silenus

Varying types of reproductive coordination among females have been described for several mammals. Among nonhuman primates, female reproductive coordination has usually been described as breeding seasonality, or in few cases, closer synchrony within the breeding or birth season. We examined birth records from a large captive colony of lion-tailed macaques, Macaca silenus, a nonseasonally breeding species, in order to determine the degree of female reproductive synchrony in this population. Births were nonrandomly distributed over the 10-year study period. Of the total of 28 births, the majority (21 or 75 %) of births occurred in cohorts, in spite of wide variations in interbirth intervals among cohort birth mothers. Cohorts consisted of two to five infants born within a 90-d period or less. Of the remaining 7 “isolated” births, four were in the three years in which only one or two births occurred. The pattern of cohort births was nonrandomly distributed according to mother's parity: three of the isolated births were to primiparous mothers, whereas only one of the 21 cohort births was to a primiparous mother. Estrous synchrony results showed that females in the longer-established of two groups exhibited greater synchrony, suggesting social facilitation of reproductive coordination. It is thus suggested that synchrony in this sample was the result of social rather than ecological mechanisms, as has been hypothesized for some other mammalian species.     

Double infanticide in a free-ranging group of buffy-headed marmosets, Callithrix flaviceps

This study describes two infanticides in a free-ranging group of Callithrix flaviceps. In November 2008, four females gave birth within a period of approximately 10 days. On the day after the third birth, the new mother was attacked by an unidentified individual, resulting in the death of one of her infants due to a bite to the top of the head. Five days later, the fourth female gave birth to twins, and the next day, the more socially dominant of the breeding females was observed ingesting the head of one of these infants. All other infants survived until the end of the study. With the exception of the unusual number of births and attacks, the behaviour appeared typical of that recorded in other marmosets, where socially dominant breeding females attack the offspring of subordinates, apparently as a strategy aimed at reducing competition for the services of infant caregivers.     

Birth Timing and Behavioral Responsiveness Predict Individual Differences in the Mother–Infant Relationship and Infant Behavior During Weaning and Maternal Breeding

There is a great deal of variability in mother–infant interactions and infant behavior across the first year of life in rhesus monkeys. The current article has two specific aims: (1) to determine if birth timing predicts variability in the mother–infant relationship and infant behavior during weaning and maternal breeding, and (2) to identify predictors of infant behavior during a period of acute challenge, maternal breeding. Forty‐one mother–infant pairs were observed during weaning when infants were 4.5 months old, and 33 were followed through maternal breeding. Subjective ratings of 16 adjectives reflecting qualities of maternal attitude, mother–infant interactions, and infant attitude were factor analyzed to construct factors relating to the mother–infant relationship (Relaxed and Aggressive) and infant behavior (Positive Engagement and Distress). During weaning, late born infants were more Positively Engaged than peak born infants (ANOVA, P < 0.05); however, birth timing did not affect the mother–infant relationship factors Relaxed and Aggressive or the infant attitude factor Distress. During maternal breeding, early born infants had less Relaxed relationships with their mothers than peak or late born infants, higher Positive Engagement scores than peak or late born infants, and tended to have higher Distress scores than peak born infants (repeated‐measures ANOVA, P < 0.05). In addition, Distress scores were higher during maternal breeding than during the pre‐ and postbreeding phases. Finally, multiple regression (P < 0.05) indicated that while infant behavioral responsiveness predicted infant Positive Engagement during the acute challenge of maternal breeding, qualities of the mother–infant relationship predicted infant Distress. These data suggest that birth timing influences the patterns of mother–infant interactions during weaning and maternal breeding. Additionally, infant behavioral responsiveness and mother–infant relationship quality impact infant social engagement and affect expression, respectively. Am. J. Primatol. 74:734‐746, 2012. © 2012 Wiley Periodicals, Inc.     

Reproductive parameters of female Japanese macaques: Thirty years data from the arashiyama troops,Japan

Over a 30-year period from 1954 to 1983, 975 live births were recorded for Japanese macaque females at the Iwatayama Monkey Park, Arashiyama, Japan. Excluding unknown birth dates, primiparous mothers gave birth to 185 infants (182 cases with age of mother known) and multiparous mothers gave birth to 723 infants (603 cases with age of mother known). The peak month of birth was May with 52.3% of the total births occurring during the period. Multiparous females who had not given birth the previous year did so earlier than multiparous females who had given birth the previous year and also earlier than primiparous females. Among the females who had given birth the previous year, females whose infant had died gave birth earlier than females who had reared an infant the previous year. The offspring sex ratio (1:0.97) was not significantly different from 1:1, and revealed no consistent association with mother's age. Age-fecundity exhibited a humped curve. The annual birth rate was low at the age of 4 years but increased thereafter, ranging between 46.7% and 69.0%, at between 5 and 19 years of age, but again decreased for females between 20 and 25 years of age. Some old females displayed clear reproductive senescence. The infant mortality within the first year of age was quite low (10.3%) and the neonatal (less than 1 month old) mortality rate accounted for 49.0% of all infant deaths. There was no significant difference between the mortality rates of male and female infants. A female's rank-class had no apparent effect on the annual birth rate, infant mortality, and offspring sex ratio. These long-term data are compared with those from other primate populations.     

Population based ascertainment of twins and their siblings, born in Western Australia 1980 to 1992, through the construction and validation of a maternally linked database of siblings.

This paper describes the creation of a unique maternal identifier for use in the investigation of perinatal, postneonatal and child outcomes in relation to maternal characteristics. All Midwives' records of Western Australian (WA) births were routinely linked to registrations of births and deaths for infants born from 1980 to 1992 inclusive, then linked to WA hospital discharge data and to registries of birth defects and cerebral palsy to create a longitudinal health record for each infant. However, since each birth to a woman was recorded as a separate event, there was no way to identify siblings. Probabilistic record linkage, based on information about the mother, was used for this task. Logical inconsistencies within the data were used to test the validity of the linkages between birth records attributed to each mother. Information about the mother from other epidemiological studies and data abstracted from hospital case notes was also used to validate sibships. Linkage of the records of 310,255 births in WA during that period resulted in the formation of 181,133 sibships of one or more children. Pooling the results of all of the validation methods gave an error of 0.9%. Linkage identified 3678 sibships containing multiple births, and 305 sets of maternal twins. Ascertainment of twins and their siblings for an ongoing twin register, the WA Twin Child Health (WATCH) study, was a natural consequence of this process.     

Feasibility of successfully breeding rhesus macaques (Macaca mulatta) to obtain healthy infants year-round

Rhesus monkeys are typically seasonal breeders but can be induced to extend the timing of their mating and births under captive conditions. The following analyses evaluated the potential impact of extending their pregnancies and deliveries year-round. Birth records from a large breeding colony housed in an indoor facility with a constant 14-hr light/10-hr dark cycle were analyzed across 25 years to examine seasonal trends in monkeys that mated in one of two ways: spontaneous in social groups or with a scheduled, timed-mating protocol. The dates of delivery and birth weights for 2,084 infants were used in these analyses. Younger nulliparous females mating in social groups evinced a clear seasonal peak when birthing their first infant. However, older females, both primiparous and multiparous, could be bred continuously, which enable the birth of infants in every month of the year. Based on the live birth rate, infant birth weights, high survival rates, and the normal sex ratio of infants birthed year-round, there were no adverse effects of breeding rhesus monkeys in this way. The continuous availability of infant births can be very advantageous for many types of research programs.     

It’s All in the Timing: Birth Seasonality and Infant Survival in <Emphasis Type="BoldItalic">Eulemur rubriventer</Emphasis>

Highly seasonal breeding has been considered one of the keys to understanding Malagasy primate socioecology. Strict seasonal breeding may be particularly critical for Malagasy primates because they live in such energetically challenging seasonal environments. Lemurs also live in highly unpredictable environments, and there is growing evidence that reproductive timing may be mediated by additional factors, suggesting that more relaxed breeding seasonality is adaptive in some cases. I tested the adaptive breadth of the birth peak in Eulemur rubriventer, which breed in several different months. I describe reproduction in the species by determining the timing and extent of the birth season (period in which all births occur) and birth peak (period in which the majority of births occur); test whether relaxed reproductive seasonality might increase reproductive success by comparing infant mortality within and outside the birth peak; and model the extent to which fruit availability has an influence on the timing of reproduction. I collected birth data on 5 groups in 2003–2005, which I combined with demographic data that D. Overdorff collected from 5 focal groups and additional censused groups between 1988 and 1996. Thirty births occurred in 8 different months. Births were significantly seasonal, with a unimodal birth peak in late August/September/October, and a mean birth date of October 11. Twenty-three births (76.7%) occurred within 54 d (14.79%) of the year. No births occurred May–July, indicating that conceptions did not occur from late December through late February, and cycling (estimated using gestation length) did not occur until ca. 101 d after the austral summer solstice (December 21). Of 22 infants followed regularly, 18 were born in the birth peak, of which 2 died (11%). All 4 infants born out of season died. Based on fruit availability, I calculated a Theoretical Overlap index (T), which indicated a 3-mo window with optimal food conditions for reproduction. This window corresponded to the timing and breadth of the birth peak in Eulemur rubriventer. These results indicate that a breeding season >3 mo within a given year is not adaptive in the species, likely due in large part to the availability of fruit during key reproductive stages, particularly before breeding.     

Social behavior of infant and mother Japanese Macaques (Macaca fuscata): Effects of kinship,partner sex,and infant sex

The behavioral interactions of 22 infant and mother Japanese macaques with other group members were studied. Focal-animal observations were made from the time of each infant’s birth until 1 year of age. Infants and mothers both displayed exceedingly strong preferences for associating with matrilineal kin and, specifically, for female kin. The degree of genetic relatedness was positively correlated with levels of spatial proximity, contact, grooming, aggression, and play. Overall frequencies of interactions with nonkin were very low, and partner sex was not an important factor in interactions with nonkin. There were no significant differences between male and female infants in interactions with kin versus nonkin. There was only one significant difference between male and female infants in interactions with males versus females: female infants showed stronger preferences for initiating proximity with females over males than did male infants. Because mothers provide the focal point for infant interactions during the first year of life, we compared the behavior of infants and mothers. Mothers were the recipients of more social interactions than were infants, mothers engaged in more grooming than did infants, and infants engaged in more social play than did mothers. These findings are only partially consistent with kin-selection theory, and the inadequacies of studying matrilineal kin discrimination to test kin selection are reviewed. The near-absence of infant sex differences in associations with social partners suggests that although maternal kin other than the mother are important to infant socialization, they probably do not contribute to the development of behavioral sex differences until after the first year of life.     

Characteristic features of the reproduction of Koshima monkeys,Macaca fuscata fuscata: A summary of thirty-four years of observation

The reproductive data for Japanese monkeys,Macaca fuscata fuscata, which had been recorded for the 34 years from 1952 to 1986 on Koshima, were analyzed in terms of the influence of changes in artificial food supplies, the differences in reproductive success between females, the timing of births, and the secondary sex ratio. Koshima monkeys increased in number until 1971 when the population density was still small and artificial provisioning was copious. As described byMori (1979b), the severe reduction in artificial food supplies, which began in 1972, had an enormous deleterious effect on reproduction: the birth ratio of adult females of 5 years of age or more fell from 57% to 25%; the rate of infant mortality within 1 year of birth rose from 19% to 45%; primiparous age rose from 6 to 9 years old on average; and there was an increased death rate among adult and juvenile females. The prolonged influence of “starvation” may be seen in the significantly delayed first births of those females that were born just before the change in food supplies. When reproductive parameters are compared between the females who belonged to six lineages in the group during these periods, they were found to be rather consistent, although some individual differences can be recognized among females and subgroups. The apparent trend was that some of the most dominant females retained superior reproductive success while that of the second-ranked females has tended to diminish over the years since 1972. Such opposing trends were seen only in the most dominant lineage group and such a difference was not recognized among the females of other lineages. The difference in reproductive success is discussed in relation to both the different situations that arise because of the artificial food supplies and differences in feeding strategies. Multiparous females, after a sterile year, gave birth somewhat earlier than those who reared infants in the preceding year and, when artificial provisioning was intense, they tended to give birth a little earlier than during other periods. There is some evidence that the mortality of later-born infants was higher than that of earlier-born infants after 1972. However, this difference may not be responsible for the differential reproductive success of females since the timing of births did not differ among lineages. Furthermore, during the time when many females gave birth continuously, prior to 1972, the infant mortality did not differ with respect to the timing of births. The differences in infant mortality were not correlated with the reproductive history, parity or age of the mother, or with the sex of the infant. The secondary sex ratio varied by only a small amount, from slightly male-biased ratio (114: 100) when correlated with reproductive history, parity, age of mother, sex and survival ratio for preceding infants, timing of birth, and lineage of the female. Furthermore, the change in artificial food supplies did not cause any modifications of the secondary sex ratios, despite its enormous deleterious effect on reproduction. The secondary sex ratio of Japanese monkeys may not be influenced by the social factors mentioned.     

Factors associated with birth rate and live birth rate in multi-male breeding groups of rhesus monkeys

Reproductive records of 284 female rhesus monkeys housed in six multimale corrals at the California Primate Research Center were examined for the birth seasons 1977–1982 to determine possible associations between the probability of birth or live birth and female age, parity, origin, parturition in the previous season, infant birth date, and infant birth date in previous season. Multiple logistic regression analysis was used to identify and quantitate the effects of factors on the probability of birth or live birth, while controlling for the possibly confounding effects of other factors in the model. Females who had infants early in the previous season were 2.5 times as likely to give birth as those who had infants late in the previous season. Females with two or three previous births were 2.1 times as likely to give birth, and those with four or five previous births were 6.7 times as likely to give birth as were females with no or one previous birth. Controlling for other factors (age, parity, and timing of birth in the previous season), corralborn females were 3.3 times as likely to give birth as either wild-caught or domestic-born monkeys not native to the corrals. Domestic-born females who were not corral natives were 0.3 times as likely to have live births as wild-caught females. Births late in the season were 1.8 times as likely to result in live infants as births early in the season.     

Observation of a birth among wild toque macaques (Macaca sinica)

Most toque macaques give birth to their infants during the night when resting arboreally. Here we report on a birth that occurred in daytime (at 0916 hr) and on the ground. The mother was 7.6 years old; the birth was her second. Prepartum behaviors included lordosis, arching of the back, stretching, squatting, rolling on the ground, and anogenital self-examination. During the birth the female was isolated about 100 m from the rest of her group. The mother stood bipedally during parturition and assisted delivery with her hands. The infant was born within 2 min after first appearing at the vulva. It immediately clung to the mother’s leg and vocalized. The mother licked the infant and oriented it toward her ventrum. She resumed foraging behavior within 20 min after parturition. The infant nursed for the first time 2.25 hr after being born. The mother ate part of the placenta, but the alpha female of the group usurped and also ate a portion of it. Curious group members sniffed and looked at the infant but did not touch it.     

Reproductive seasonality in a free-ranging troop of stumptail macaques (Macaca arctoides): A five-year report

Seasonality in births and fertile matings are reported for a stumptail macaque group living on an island for a period of five years: 1975–1979. During this period 26 births occurred of which 24 represent infants conceived on the island. While births and fertile matings occurred throughout the year 21% of the births were concentrated in March, 34% in June and July and 17% in November. Additionally 63% of the births occurred during the rainy season. Of the 24 infants, 4 died during the first year of life thus yielding a reproductive success of 83%. The sex ratio at birth for the five years was 1:1 corrected to 1:1.2 with the four deaths. The mean interval between fertile matings for females was 19 months and 2 days and the mean age for first conception was 4 years and 5 months. The pattern of birth and breeding seasonality was markedly similar to that of the parent troop while in Puerto Rico.     

Mother-infant cannibalism in thick-tailed bushbabies (Galago crassicaudatus umbrosus)

Mother-infant cannibalism in species of galagos as in several other species of non-human primates is a common phenomenon. In non-human primates kept in laboratory conditions many of the observed cases of cannibalism were not associated with starvation and with infanticide. Cannibalism in galagos was observed in at least five different species. In several laboratories, like the Duke University Primate Center, the frequencies of cannibalism in galagos species in captivity have been reduced by the isolation of pregnant female before the parturition from her companions, especially adult males. At the Primate Behaviour Research Group (University of Witwatersrand, Johannesburg, South Africa) three cases of cannibalism were observed in twoGalago crassicaudatus umbrosus' mothers before the end of the third day after birth. To understand the reasons why the mothers cannibalize their own infants, it was decided to analyze the mother-infant interaction which preceded the death of the infants. InGalago crassicaudatus twin and triplet births are very common. In one of our two observed mothers who cannibalized their infants, there was one triplet birth. In this study the two pregnant females were isolated in two separated cages ten days before giving birth. One of the two observed mothers gave birth to triplets, the other had a single birth. At the end all four infants were cannibalized. In all cases the cannibalization started after the infant's death. The infants' deaths were caused by lack of maternal care which caused them to starve. The results show that the triplet's mother differed in some of her behaviour towards her infants. In one of the cannibalized infants behaviours such asNipple andMother Passive Prevent were never seen before death. In our cases it seems that cannibalism was probably due to the laboratory condition that for generation to generation caused stress to the mothers and changed their maternal behaviours, which lead to the death of the offspring which after death became a consumable resource.     

Infant carrying in family groups of goeldi's monkeys (Callimico goeldii)

Goeldi's monkey (Callimico goeldii) is closely related to marmosets and tamarins. Like marmosets and tamarins, C. goeldii lives in family groups, and fathers and older offspring (helpers) participate in infant carrying. In contrast to the typical twin births in marmosets and tamarins, C. goeldii has only single offspring, and paternal carrying is delayed. We studied infant carrying following 26 births in eight groups of C. goeldii, testing hypotheses proposed in the literature on infant carrying in marmosets and tamarins. The infant was carried exclusively by the mother for the first 26.3 days after birth. Afterwards other group members participated in infant carrying. Whereas the C. goeldii mother is always the main carrier, the father does not always carry more than helpers. In contrast to other callitrichids, age and sex of sibling helpers was not found to have an effect on the participation in infant carrying. The participation in infant carrying in Callimico indicated intraindividual consistency, i.e., the amount of infant carrying performed by fathers and helpers following one birth correlated significantly with the amount of infant carrying of the same individuals following the next birth. We found a significant negative correlation between parental infant carrying and group size, indicating that helpers really do help, sharing the carrying burden with their parents. This is attributed to a clear trend for a reduction in maternal carrying in the presence of helpers, whereas fathers did not benefit from helpers. We conclude that the infant-carrying pattern in C. goeldii is different from the infant-carrying pattern in marmosets and tamarins. The main differences were that the mother instead of the father is the main carrier, and that there is a clear time delay between infant birth and when the father and helpers participate in infant carrying.     

Reproduction in the slow loris (Nycticebus coucang)

The reproductive biology of the slow loris (Nycticebus coucang) is poorly documented because of infrequent captive breeding success and the absence of field studies of this species. Reproductive data were collected from a breeding colony of slow lorises held at the Duke University Primate Center for the past 10 years. Nineteen infants were born, with a sex ratio of 1:1 and a neonatal mortality rate of 15.8%. In all cases, litter size was one. Females born in the colony copulated for the first time between 18 and 24 months of age. A male that reached sexual maturity in the colony sired his first offspring at the age of 17 months. Estrous cycles ranged in duration from 29–45 days, with copulations usually occurring for 1 day of estrus. Gestation length averaged 192.2 days. Although a postpartum estrus was observed in three cases of infant death, no conceptions resulted. Lactation lasted approximately 6 months. A clear birth peak was observed, with 12 out of 19 births occurring in March, April, and May. The comparatively low basal metabolic rate of this species may account for the unusually low reproductive rate of the slow loris in comparison with other prosimian primates.     

Pediatric paradox: heterogeneity in the birth cohort

Comparisons of birth-weight-specific infant mortality indicate that low-birth-weight African American infants have lower mortality than low-birth-weight European American infants despite higher infant mortality overall-the "pediatric paradox." One explanation is heterogeneity in birth weight. Analyses of African American and European American births suggest that birth cohorts consist of two heterogeneous subpopulations. One appears to account for normal births, whereas the other may consist of compromised births. Estimates of infant mortality indicate that the compromised subpopulation has higher overall mortality but lower birth-weight-specific mortality. We attribute lower birth-weight-specific infant mortality in the compromised subpopulation to higher rates of fetal loss. Compared to European American birth cohorts, African American birth cohorts have (1) higher birth-weight-specific mortality in the normal subpopulation, (2) larger compromised subpopulations, and (3) lower birth-weight-specific mortality in the compromised subpopulation. Consequently, the pediatric paradox is attributable to greater rates of compromised pregnancies and higher fetal losses among African Americans.     

Life history variables of wild troops of formosan macaques (Macaca cyclopis) in Kenting,Taiwan

A study on population dynamics of wild Formosan macaques (Macaca cyclopis) in Kenting, southern Taiwan, was conducted from March 1985 to August 1990. At first, only one monkey troop was studied. It fissioned in 1987 and both of the daughter troops have been observed since then. Total number of animals increased from 10 to 29 over the years, but the sizes of individual troops have never been more than 20. Seasonality in breeding has been detected: copulations were concentrated in the period from November to January and 75% of all the 28 births occurred between April and June. Time of birth by parous females without offspring from the preceding year was earlier than that of lactating females. Young females gave their first births at 4 or 5 years of age. Total birth rate over the study period was 0.8 infant per female per year. Hunting was the main cause of death while natural mortality rate was low for the animals. There was only one adult male in each troop for most of the time. Troop males in the two daughter troops have been replaced two or three times in the three years by some solitary males that moved around in the area. The reproductive parameters of Formosan macaques in Kenting were found to be more similar to that of rhesus monkeys than to Japanese macaques. And a case of higher reproductive success in a high-ranking matriline was reported.     

Lactation and care for unrelated infants in forest-living ringtailed Lemurs

An adult female ringtailed lemur (Lemur catta) known not to have been pregnant showed spontaneous lactation in response to twin infants born to an unrelated female. The females had met only 7 months earlier, when they and two other unrelated adult females were released from separate locations in a forest enclosure to form a new social group. Three months after release, an adult male from an adjacent enclosure gained access to the new group for 1 day, the day of one female's estrus. No males had access to the females throughout the remainder of the breeding season. Within 2 weeks of the birth of the twins, one of the other adult females began carrying the infants frequently, typically one at a time. All three females were checked for lactation when the infants were two months old. Both their mother and the unrelated adult who had been carrying the infants were producing milk. The third adult female, who never carried either infant, had no milk. The third adult female, who never carried either infant, had no milk. This female, however, like the two maternal females, frequently attacked unfamiliar immigrating adult males when the males approached the infants. Potential implications of these observations concerning the social organization of ringtailed lemurs are discussed.     

Male-infant relationships in semifree-ranging Barbary macaques (Macaca sylvanus) of affenberg salem/FRG: Testing the “male care” hypothesis

The infant-directed behavior of Barbary macaque males was analyzed in order to determine whether it is essential for an infant's survival during the first year and whether males interact selectively with closely related infants. Dyadic male-infant contacts were recorded in a large group of semifree-ranging Barbary macaques. Data collected during the first 12 weeks of life on each infant born in 1983 (n = 36) were analyzed. All adult and almost all subadult males established strong relationships with at least one infant. Almost two-thirds of the infants (22) had frequent contacts with one or several males. Males showed no preference for closely related infants. Sexual associations with an infant's mother during the preceding mating season had no significant effect. Natal males did not prefer infants of their own matrilineage. There was no evidence that contacts with males had a positive influence on infant survival or that other benefits to the infants resulted from these contacts. Instead, excessive carrying by males and females led to starvation of some very young infants and was a major cause of neonatal deaths in this population. Males interacted preferentially with infants that were born early in the birth season, had a high-ranking multiparous mother, and were male. Younger males established strong relationships with male infants only, while mother's rank was more important for older males. It is suggested that certain mothers prevented early contacts between their infants and males so that the observed preferences for certain infants were also a result of easier access to them. All results suggested that males interacted with infants for their own benefit.